Osteoporosis Associated with Breast Cancer Treatments Based on Types of Hormonal Therapy: A Cross-Sectional Study Using Korean National Sample Data
Abstract
:1. Introduction
2. Materials and Methods
2.1. Data Source
2.2. Study Design and Population
2.3. Study Covariates
2.4. Statistical Analysis
3. Results
3.1. Patient Characteristics
3.2. Hormone Therapy Prescriptions
3.3. Prescribing Trends of Anticancer Medications
4. Discussion
Strengths and Limitations
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- De Cicco, P.; Catani, M.V.; Gasperi, V.; Sibilano, M.; Quaglietta, M.; Savini, I. Nutrition and breast cancer: A literature review on prevention, treatment and recurrence. Nutrients 2019, 11, 1514. [Google Scholar] [CrossRef] [PubMed]
- Bray, F.; Ferlay, J.; Soerjomataram, I.; Siegel, R.L.; Torre, L.A.; Jemal, A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 2018, 68, 394–424. [Google Scholar] [CrossRef] [PubMed]
- Houghton, S.C.; Hankinson, S.E. Cancer progress and priorities: Breast cancer. Cancer Epidemiol. Biomark. Prev. 2021, 30, 822–844. [Google Scholar] [CrossRef] [PubMed]
- Allemani, C.; Matsuda, T.; Di Carlo, V.; Harewood, R.; Matz, M.; Nikšić, M.; Bonaventure, A.; Valkov, M.; Johnson, C.J.; Estève, J. Global surveillance of trends in cancer survival 2000–14 (CONCORD-3): Analysis of individual records for 37 513 025 patients diagnosed with one of 18 cancers from 322 population-based registries in 71 countries. Lancet 2018, 391, 1023–1075. [Google Scholar] [CrossRef] [PubMed]
- Kang, S.Y.; Kim, Y.S.; Kim, Z.; Kim, H.-Y.; Lee, S.K.; Jung, K.-W.; Youn, H.J.; Society, K.B.C. Basic findings regarding breast cancer in Korea in 2015: Data from a breast cancer registry. J. Breast Cancer 2018, 21, 1–10. [Google Scholar] [CrossRef] [PubMed]
- Chen, Z.; Maricic, M.; Pettinger, M.; Ritenbaugh, C.; Lopez, A.M.; Barad, D.H.; Gass, M.; LeBoff, M.S.; Bassford, T.L. Osteoporosis and rate of bone loss among postmenopausal survivors of breast cancer: Results from a subgroup in the Women’s Health Initiative Observational Study. Cancer 2005, 104, 1520–1530. [Google Scholar] [CrossRef] [PubMed]
- Kim, Y.A.; Oh, I.-H.; Yoon, S.-J.; Kim, H.-J.; Seo, H.-Y.; Kim, E.-J.; Lee, Y.H.; Jung, J.H. The economic burden of breast cancer in Korea from 2007–2010. Cancer Res. Treat. Off. J. Korean Cancer Assoc. 2015, 47, 583–590. [Google Scholar] [CrossRef] [PubMed]
- Akram, M.; Iqbal, M.; Daniyal, M.; Khan, A.U. Awareness and current knowledge of breast cancer. Biol. Res. 2017, 50, 33. [Google Scholar] [CrossRef]
- Hortobagyi, G.N. Treatment of breast cancer. N. Engl. J. Med. 1998, 339, 974–984. [Google Scholar] [CrossRef]
- Reinert, T.; de Paula, B.; Shafaee, M.N.; Souza, P.H.; Ellis, M.J.; Bines, J. Endocrine therapy for ER-positive/HER2-negative metastatic breast cancer. Chin. Clin. Oncol. 2018, 7, 25. [Google Scholar] [CrossRef]
- Khosrow-Khavar, F.; Filion, K.; Al-Qurashi, S.; Torabi, N.; Bouganim, N.; Suissa, S.; Azoulay, L. Cardiotoxicity of aromatase inhibitors and tamoxifen in postmenopausal women with breast cancer: A systematic review and meta-analysis of randomized controlled trials. Ann. Oncol. 2017, 28, 487–496. [Google Scholar] [CrossRef] [PubMed]
- Bradley, R.; Braybrooke, J.; Gray, R.; Hills, R.K.; Liu, Z.; Pan, H.; Peto, R.; Dodwell, D.; McGale, P.; Taylor, C. Aromatase inhibitors versus tamoxifen in premenopausal women with oestrogen receptor-positive early-stage breast cancer treated with ovarian suppression: A patient-level meta-analysis of 7030 women from four randomised trials. Lancet Oncol. 2022, 23, 382–392. [Google Scholar] [CrossRef] [PubMed]
- Aleanizy, F.S.; Alqahtani, F.Y.; Seto, S.; Al Khalil, N.; Aleshaiwi, L.; Alghamdi, M.; Alquadeib, B.; Alkahtani, H.; Aldarwesh, A.; Alqahtani, Q.H. Trastuzumab targeted neratinib loaded poly-amidoamine dendrimer nanocapsules for breast cancer therapy. Int. J. Nanomed. 2020, 15, 5433. [Google Scholar] [CrossRef] [PubMed]
- Dean, L.; Kane, M. Pertuzumab Therapy and ERBB2 Genotype. In Medical Genetics Summaries; National Center for Biotechnology Information (US): Bethesda, MD, USA, 2021. [Google Scholar]
- Barok, M.; Joensuu, H.; Isola, J. Trastuzumab emtansine: Mechanisms of action and drug resistance. Breast Cancer Res. 2014, 16, 209. [Google Scholar] [CrossRef] [PubMed]
- Huang, X.-J.; Li, X.-Y.; Li, J.-H.; Hu, Z.-Y.; Luo, L.; Tan, Y.; Chen, H.-Y.; Fan, R.-R.; Wang, T.-Y.; Meng, L.-Q. Nomogram for Predicting Chemotherapy-Induced Nausea and Vomiting for Breast Cancer Patients. Tohoku J. Exp. Med. 2021, 254, 111–121. [Google Scholar] [CrossRef] [PubMed]
- Wesmiller, S.W.; Bender, C.M.; Conley, Y.P.; Bovbjerg, D.H.; Ahrendt, G.; Bonaventura, M.; Sereika, S.M. A prospective study of nausea and vomiting after breast cancer surgery. J. PeriAnesthesia Nurs. 2017, 32, 169–176. [Google Scholar] [CrossRef] [PubMed]
- Johnsson, A.; Demmelmaier, I.; Sjövall, K.; Wagner, P.; Olsson, H.; Tornberg, Å.B. A single exercise session improves side-effects of chemotherapy in women with breast cancer: An observational study. BMC Cancer 2019, 19, 1073. [Google Scholar] [CrossRef]
- Lindsey, A.M.; Gross, G.; Twiss, J.; Waltman, N.; Ott, C.; Moore, T.E. Postmenopausal survivors of breast cancer at risk for osteoporosis: Nutritional intake and body size. Cancer Nurs. 2002, 25, 50–56. [Google Scholar] [CrossRef]
- Hadji, P. Aromatase inhibitor-associated bone loss in breast cancer patients is distinct from postmenopausal osteoporosis. Crit. Rev. Oncol./Hematol. 2009, 69, 73–82. [Google Scholar] [CrossRef]
- Coleman, R.E.; Body, J.J.; Gralow, J.R.; Lipton, A. Bone loss in patients with breast cancer receiving aromatase inhibitors and associated treatment strategies. Cancer Treat. Rev. 2008, 34 (Suppl. S1), S31–S42. [Google Scholar] [CrossRef]
- Sakaguchi, K.; Ono, H.; Nakatsukasa, K.; Ishikawa, T.; Hasegawa, Y.; Takahashi, M.; Niikura, N.; Koizumi, K.; Sakurai, T.; Shigematsu, H. Efficacy of denosumab for restoring normal bone mineral density in women receiving adjuvant aromatase inhibitors for early breast cancer. Medicine 2019, 98, e16770. [Google Scholar] [CrossRef] [PubMed]
- Nicolatou-Galitis, O.; Schiødt, M.; Mendes, R.A.; Ripamonti, C.; Hope, S.; Drudge-Coates, L.; Niepel, D.; Van den Wyngaert, T. Medication-related osteonecrosis of the jaw: Definition and best practice for prevention, diagnosis, and treatment. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. 2019, 127, 117–135. [Google Scholar] [CrossRef] [PubMed]
- Suarez-Almazor, M.E.; Herrera, R.; Lei, X.; Chavez-MacGregor, M.; Zhao, H.; Giordano, S.H. Survival in older women with early stage breast cancer receiving low-dose bisphosphonates or denosumab. Cancer 2020, 126, 3929–3938. [Google Scholar] [CrossRef] [PubMed]
- Biskup, E.; Cai, F.; Vetter, M. Bone targeted therapies in advanced breast cancer. Swiss Med. Wkly. 2017, 147, w14440. [Google Scholar] [CrossRef] [PubMed]
- Kelly, E.; Lu, C.Y.; Albertini, S.; Vitry, A. Longitudinal trends in utilization of endocrine therapies for breast cancer: An international comparison. J. Clin. Pharm. Ther. 2015, 40, 76–82. [Google Scholar] [CrossRef] [PubMed]
- Kim, L.; Kim, J.-A.; Kim, S. A guide for the utilization of health insurance review and assessment service national patient samples. Epidemiol. Health 2014, 36, e2014008. [Google Scholar] [CrossRef] [PubMed]
- Park, Y.J.; Kim, H.S.; Kang, H.C. The age at menopause and related factors in Korean women. J. Korean Acad. Nurs. 2002, 32, 1024–1031. [Google Scholar] [CrossRef]
- Heer, E.; Harper, A.; Escandor, N.; Sung, H.; McCormack, V.; Fidler-Benaoudia, M.M. Global burden and trends in premenopausal and postmenopausal breast cancer: A population-based study. Lancet Glob. Health 2020, 8, e1027–e1037. [Google Scholar] [CrossRef]
- Nam, G.E.; Kim, Y.-H.; Han, K.; Jung, J.-H.; Rhee, E.-J.; Lee, S.-S.; Kim, D.J.; Lee, K.-W.; Lee, W.-Y. Obesity fact sheet in Korea, 2019: Prevalence of obesity and abdominal obesity from 2009 to 2018 and social factors. J. Obes. Metab. Syndr. 2020, 29, 124. [Google Scholar] [CrossRef]
- Fallowfield, L.; Osborne, S.; Langridge, C.; Monson, K.; Kilkerr, J.; Jenkins, V. Implications of subcutaneous or intravenous delivery of trastuzumab; further insight from patient interviews in the PrefHer study. Breast 2015, 24, 166–170. [Google Scholar] [CrossRef]
- De Cock, E.; Pivot, X.; Hauser, N.; Verma, S.; Kritikou, P.; Millar, D.; Knoop, A. A time and motion study of subcutaneous versus intravenous trastuzumab in patients with HER 2-positive early breast cancer. Cancer Med. 2016, 5, 389–397. [Google Scholar] [CrossRef] [PubMed]
- Johnson, R.H.; Anders, C.K.; Litton, J.K.; Ruddy, K.J.; Bleyer, A. Breast cancer in adolescents and young adults. Pediatr. Blood Cancer 2018, 65, e27397. [Google Scholar] [CrossRef] [PubMed]
- Avci, O.; Tacar, S.Y.; Seber, E.S.; Yetisyigit, T. Breast cancer in young and very young women; Is age related to outcome? J. Cancer Res. Ther. 2021, 17, 1322. [Google Scholar]
- Kim, J.; Hong, S.; Lee, J.J.; Won, Y.-J.; Lee, E.S.; Kang, H.-S.; Lee, S.; Han, J.H.; Lee, E.-G.; Jo, H. Analysis of the tumor characteristics in young age breast cancer patients using collaborative stage data of the Korea Central Cancer Registry. Breast Cancer Res. Treat. 2021, 187, 785–792. [Google Scholar] [CrossRef] [PubMed]
- Lambertini, M.; Ceppi, M.; Cognetti, F.; Cavazzini, G.; De Laurentiis, M.; De Placido, S.; Michelotti, A.; Bisagni, G.; Durando, A.; Valle, E. Dose-dense adjuvant chemotherapy in premenopausal breast cancer patients: A pooled analysis of the MIG1 and GIM2 phase III studies. Eur. J. Cancer 2017, 71, 34–42. [Google Scholar] [CrossRef] [PubMed]
- Kim, M.; Kim, H.; Ahn, S.H.; Tabatabaie, V.; Choi, S.W.; Sohn, G.; Lee, S.B.; Ko, B.S.; Chung, I.Y.; Kim, J. Changes in bone mineral density during 5 years of adjuvant treatment in premenopausal breast cancer patients. Breast Cancer Res. Treat. 2020, 180, 657–663. [Google Scholar] [CrossRef] [PubMed]
- Elkin, E.B.; Marshall, D.A.; Kulin, N.A.; Ferrusi, I.L.; Hassett, M.J.; Ladabaum, U.; Phillips, K.A. Economic evaluation of targeted cancer interventions: Critical review and recommendations. Genet. Med. 2011, 13, 853–860. [Google Scholar] [CrossRef] [PubMed]
- Masuda, T.; Fujimoto, H.; Teranaka, R.; Kuroda, M.; Aoyagi, Y.; Nagashima, T.; Sangai, T.; Takada, M.; Nakagawa, A.; Kubota, Y. Anti-HER2 antibody therapy using gene-transduced adipocytes for HER2-positive breast cancer. Breast Cancer Res. Treat. 2020, 180, 625–634. [Google Scholar] [CrossRef]
- Choe, S.-A.; Sung, J. Trends of premature and early menopause: A comparative study of the US National Health and Nutrition Examination Survey and the Korea National Health and Nutrition Examination Survey. J. Korean Med. Sci. 2020, 35, e97. [Google Scholar] [CrossRef]
- Dall, G.V.; Britt, K.L. Estrogen effects on the mammary gland in early and late life and breast cancer risk. Front. Oncol. 2017, 7, 110. [Google Scholar] [CrossRef]
- Reinert, T.; Barrios, C.H. Optimal management of hormone receptor positive metastatic breast cancer in 2016. Ther. Adv. Med. Oncol. 2015, 7, 304–320. [Google Scholar] [CrossRef]
- Sharma, G.N.; Dave, R.; Sanadya, J.; Sharma, P.; Sharma, K. Various types and management of breast cancer: An overview. J. Adv. Pharm. Technol. Res. 2010, 1, 109. [Google Scholar]
Category | Overall Cohort | Non-OSP | OSP | p-Value * | |||
---|---|---|---|---|---|---|---|
No. of Patients | % | No. of Patients | % | No. of Patients | % | ||
Age (years) | <0.0001 | ||||||
<35 | 648 | 2.17 | 563 | 2.61 | 85 | 1.03 | |
35–44 | 4673 | 15.65 | 4001 | 18.54 | 672 | 8.12 | |
45–54 | 11,113 | 37.22 | 8678 | 40.20 | 2435 | 29.43 | |
55–64 | 8444 | 28.28 | 5622 | 26.05 | 2822 | 34.11 | |
65–74 | 3719 | 12.46 | 2020 | 9.36 | 1699 | 20.54 | |
≥75 | 1261 | 4.22 | 701 | 3.25 | 560 | 6.77 | |
Sex | <0.0001 | ||||||
Male | 120 | 0.40 | 107 | 0.50 | 13 | 0.16 | |
Female | 29,738 | 99.60 | 21,478 | 99.50 | 8260 | 99.84 | |
Anticancer | |||||||
SERMs | 8949 | 29.97 | 6803 | 31.52 | 2146 | 25.94 | <0.0001 |
Aromatase Inhibitors | 6221 | 20.84 | 3385 | 15.68 | 2836 | 34.28 | <0.0001 |
Cytotoxic anticancer | 4387 | 14.69 | 3187 | 14.76 | 1200 | 14.51 | 0.570 |
Targeted anticancer | 1735 | 5.81 | 1211 | 5.61 | 524 | 6.33 | 0.017 |
Others | 1502 | 5.03 | 1123 | 5.20 | 379 | 4.58 | 0.028 |
Payer type | <0.0001 | ||||||
NHI | 28,430 | 95.22 | 20,656 | 95.70 | 7774 | 93.97 | |
Medicaid | 1427 | 4.78 | 928 | 4.30 | 499 | 6.03 | |
Others | 1 | 0.00 | 1 | 0.00 | - | - | |
Year | 0.491 | ||||||
2010 | 2155 | 7.22 | 1555 | 7.20 | 600 | 7.25 | |
2011 | 2205 | 7.38 | 1579 | 7.32 | 626 | 7.57 | |
2012 | 2365 | 7.92 | 1731 | 8.02 | 634 | 7.66 | |
2013 | 2559 | 8.57 | 1843 | 8.54 | 716 | 8.65 | |
2014 | 2728 | 9.14 | 1967 | 9.11 | 761 | 9.20 | |
2015 | 3006 | 10.07 | 2194 | 10.16 | 812 | 9.82 | |
2016 | 3170 | 10.62 | 2321 | 10.75 | 849 | 10.26 | |
2017 | 3620 | 12.12 | 2639 | 12.23 | 981 | 11.86 | |
2018 | 3867 | 12.95 | 2740 | 12.69 | 1127 | 13.62 | |
2019 | 4183 | 14.01 | 3016 | 13.97 | 1167 | 14.11 | |
Compound annual growth rate | 7.65% | 7.64% | 7.67% |
Overall Cohort | Non-OSP (<55 Years) | OSP (<55 Years) | Non-OSP (≥55 Years) | OSP (≥55 Years) | ||||||
---|---|---|---|---|---|---|---|---|---|---|
Anticancer Categories | No. of Patients (ACR) | Costs (ACR) | No. of Patients (ACR) | Costs (ACR) | No. of Patients (ACR) | Costs (ACR) | No. of Patients (ACR) | Costs (ACR) | No. of Patients (ACR) | Costs (ACR) |
SERMs | 895 (6.21%) | USD 179,295 (1.80%) | 588 (6.61%) | USD 111,607 (2.66%) | 133 (4.61%) | USD 25,662 (−0.80%) | 92 (3.13%) | USD 20,813 (−4.09%) | 62 (6.46%) | USD 17,871 (3.69%) |
Aromatase Inhibitors | 622 (8.68%) | USD 549,646 (4.14%) | 103 (2.83%) | USD 88,607 (−0.59%) | 73 (2.67%) | USD 63,709 (−2.52%) | 236 (12.44%) | USD 207,035 (7.52%) | 211 (9.82%) | USD 190,295 (5.05%) |
Cytotoxic anticancer | 439 (2.88%) | USD 775,687 (−1.40%) | 219 (−0.16%) | USD 373,969 (−2.95%) | 63 (0.37%) | USD 135,476 (−6.88%) | 100 (7.78%) | USD 168,012 (1.89%) | 57 (7.70%) | USD 97,503 (4.03%) |
Other anticancer | 150 (11.72%) | USD 243,773 (9.99%) | 108 (12.83%) | USD 166,451 (9.21%) | 35 (6.27%) | USD 59,537 (6.01%) | 05 (17.88%) | USD 11,055 (69.15%) | 29 (11.97%) | USD 17,107 (37.15%) |
Targeted anticancer | 174 (16.11%) | USD 2,294,696 (16.37%) | 75 (13.41%) | USD 998,046 (11.94%) | 26 (11.17%) | USD 357,198 (16.70%) | 46 (21.22%) | USD 615,249 (21.23%) | 27 (22.90%) | USD 317,867 (21.98%) |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Wang, Y.M.; Lim, Y.-C.; Hwang, D.-S.; Lee, Y.J.; Ha, I.-H.; Lee, Y.-S. Osteoporosis Associated with Breast Cancer Treatments Based on Types of Hormonal Therapy: A Cross-Sectional Study Using Korean National Sample Data. Medicina 2023, 59, 1505. https://doi.org/10.3390/medicina59091505
Wang YM, Lim Y-C, Hwang D-S, Lee YJ, Ha I-H, Lee Y-S. Osteoporosis Associated with Breast Cancer Treatments Based on Types of Hormonal Therapy: A Cross-Sectional Study Using Korean National Sample Data. Medicina. 2023; 59(9):1505. https://doi.org/10.3390/medicina59091505
Chicago/Turabian StyleWang, Yen Min, Yu-Cheol Lim, Deok-Sang Hwang, Yoon Jae Lee, In-Hyuk Ha, and Ye-Seul Lee. 2023. "Osteoporosis Associated with Breast Cancer Treatments Based on Types of Hormonal Therapy: A Cross-Sectional Study Using Korean National Sample Data" Medicina 59, no. 9: 1505. https://doi.org/10.3390/medicina59091505